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Downloaded from Bioscientifica.Com at 09/28/2021 08:12:18PM Via Free Access 678 L Reproduction (2001) 121, 677–683 Review Mechanisms for pattern formation leading to axis formation and lineage allocation in mammals: a marsupial perspective Lynne Selwood Department of Zoology, University of Melbourne, Royal Parade, 3010 Vic, Australia Developing patterns in early embryogenesis are analysed in conceptuses from several families, including Dasyuridae, Phalangeridae, Macropodidae and Didelphidae, in which cleavage has been examined in some detail. Features common to cleavage and blastocyst formation, and in some cases to hypoblast formation, are used to develop an outline of possible mechanisms leading to axis formation and lineage allocation. Relevant features that have been described only in some species are also included. It is suggested that certain features of marsupial cleavage establish patterns in the developing blastocyst epithelia, pluriblast, trophoblast and hypoblast that contribute to axis formation and lineage allocation. All marsupials examined had a polarized oocyte or conceptus, the polarity of which was related to the conceptus embryonic–abembryonic axis and, eventually, the conceptus dorsal–ventral axis and the formation of the pluriblast (future embryo) and trophoblast. The embryonic dorsal–ventral and anterior–posterior axes were established after the allocation of hypoblast and epiblast. Mechanisms that appear to result in patterning of the developing epithelia leading to axis formation and lineage allocation are discussed, and include sperm entry point, gravity, conceptus polarity, differentials in cell–zona, cell–cell and cell-type (boundary effects) contacts, cell division order during cleavage and signals external to the conceptus. A model of the patterning effects is included. The applicability of these mechanisms to other amniotes, including eutherian mammals, is also examined. Because of the simplified nature of blastocyst formation, environment by development of a placenta. This review will study of marsupial development has the potential to give show how a study of early marsupial development reveals insights into developmental mechanisms and evolution of potential mechanisms for lineage allocation and axis the mammalian embryo, especially with respect to axis formation. formation and lineage allocation. Marsupials do not form a morula but instead the blastomeres undergo a mesenchyme– Conceptus and embryonic axes epithelial transformation during cleavage to form a unilaminar epithelium in which both the pluriblast (equiv- In amniotes, because early processes are concerned with alent to the inner cell mass; ICM) and the trophoblast are establishing the extra-embryonic lineages and the embryo superficial in position. The terminology of Johnson and proper does not emerge until later, it is important to distinguish Selwood (1996), which allows equivalent structures in between axes developing with respect to the conceptus and different mammalian groups to be compared, is used in this those developing with respect to the embryo proper. The two review. axes are related but are not exactly the same (Fig. 1). Axis Marsupial studies may indicate some evolutionary formation and lineage allocation are intimately related in all processes because marsupial conceptuses have features in amniotes in which the separation of embryonic from extra- common with other amniotes. Like the conceptus of reptiles embryonic lineages is preceded by the establishment of the and birds the marsupial conceptus is covered by a number conceptus embryonic–abembryonic axis (E/AbE). The first of egg coats. The mode of formation of the early embryonic extra-embryonic lineages, trophoblast or extra-embryonic and extra-embryonic lineages is remarkably similar to that ectoderm of the yolk sac and then hypoblast (Fig. 1), have found in reptiles and birds, but can be readily seen because fundamental roles in conceptus nourishment and embryonic of the paucity of yolk material. Like the conceptus of signalling. They also are manifestations of the first signs of the eutherian mammals, the marsupial conceptus has to emerging dorsal–ventral (D–V) axis for the conceptus as a prepare itself to obtain nourishment from the uterine whole (Fig. 1). Within the epiblast, which gives rise to the future embryo (Johnson and Selwood, 1996), the definitive Email: [email protected] embryonic D–V and anterior–posterior (A–P) axes of the future © 2001 Journals of Reproduction and Fertility 1470-1626/2001 Downloaded from Bioscientifica.com at 09/28/2021 08:12:18PM via free access 678 L. Selwood Table 1. Possible mechanisms leading to axial gradients or lineage allocation in marsupials Mechanisms Evidence References Uneven distribution of determinants Oocyte or zygote polarity Selwood and Hickford, 1999 (review) Gravity Gravity-related orientation of conceptuses Baggott and Moore, 1990 in one species Sperm entry point Identified in some species showing marked Merry et al., 1995; Selwood, unpublished oocyte polarity before fertilization Cleavage patterns Stylized and specific morphology Selwood, 1992 Intrinsic signals Cell division order creates pattern in Selwood and Smith, 1990 pluriblast and trophoblast Extrinsic signals Developmental arrests in vitro Selwood, 1992 (review) organism emerges (Fig. 1). Apart from the small size, the nants. Direct determinants are defined as determinants the appearance of the marsupial epiblast during gastrulation is presence of which results directly in axial gradients or similar to that of birds, reptiles and monotremes. lineage allocation. Indirect or pattern-forming determinants are determinants the presence of which creates a pattern leading eventually to axial gradients or lineage allocation. Possible mechanisms leading to axial gradients or Polarity may be related to the uneven distribution of direct lineage allocation determinants because the conceptus E/AbE, D–V axis and It is proposed here that axial gradients are set up during the first lineage allocation into pluriblast and trophoblast early development before the axis can be detected mor- appears to be related to the cytoplasmic polarity of the phologically. The processes in marsupials that have the zygote (Fig. 1). The fact that the differences between potential to create patterns in the developing blastocyst pluriblast and trophoblast often disappear soon after the epithelium leading to either axial gradients or lineage blastocyst epithelium is complete (one or two cell divisions) allocation, or both, are discussed below (see Table 1). does not support this contention and indicates that polarity is more likely to be related to the distribution of indirect Conceptus axis formation and pluriblast–trophoblast determinants to ensure that formation of the blastocyst allocation epithelium is localized to one hemisphere. These two alternatives need to be tested experimentally. After cell– Oocyte–zygote polarity. Oocyte–zygote polarity is a zona adhesion begins (Fig. 2), polarity in trophoblast and feature encountered commonly in most marsupial families pluriblast cells becomes related to the blastocyst epithelium, (Figs 1 and 2) and is expressed in the eccentric location of the outer surface of which is apical (Frankenberg and the nucleus or other organelles in oocytes and cleavage Selwood, 1998). This process is in contrast to that in stage conceptuses, the polarized discharge of pale vesicles eutherian mammals, in which only trophoblast cells are releasing an extracellular matrix (ECM) into the cleavage polarized. cavity or vesicles associated with cell–zona adhesion, the polarized nature of cell–zona adhesion, which is always Sperm entry point. Sperm entry point appears to occur localized initially to the hemisphere opposite vesicle preferentially in the hemisphere opposite the accumulation emission (Fig. 3b) and the asymmetric mucoid coat in some of vesicles that contribute to the yolk mass in dasyurid species (Selwood and Hickford, 1999). All early concep- marsupials (Table 1) and within 60Њ of the position of the tuses show polarity but do not all share the same polarized first polar body (Fig. 3). This preference may occur because features. However, all early conceptuses that have been penetration in the hemisphere containing the vesicular analysed ultrastructurally show polarity related to the material of the future yolk mass makes migration of the distribution of vesicles at one pole and nucleus or sperm head difficult or impossible. If the relationship mitochondrial-rich cytoplasm at the other (Selwood and between oocyte polarity, sperm entry point and the future Sathananthan, 1988; Baggott and Moore, 1990; Renfree D–V axis is examined in dasyurids, some parallels with the and Lewis, 1996; Frankenberg and Selwood, 1998). A relationship in the frog can be seen (Fig. 3) that indicate that variety of anchoring devices characterize marsupial zygotes the sperm entry point may be associated with formation of so that the mitochondrial-rich cytoplasm is retained when the conceptus D–V axis. This hypothesis needs to be tested vesicles or the yolk mass are discharged (Breed et al., 1994, experimentally. If the sperm entry point is demonstrated to 1995; Merry et al., 1995; Frankenberg and Selwood, 1998). play a role in conceptus D–V axis formation, the move- Oocyte polarity may be related to polarized distribution ments of the cytoplasm after fertilization may be in response of either direct determinants or indirect maternal determi- to a gravitational stimulus (Table 1). Downloaded from Bioscientifica.com at 09/28/2021 08:12:18PM via free access
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